Mycotoxins and other fungal metabolites in grain dust from Norwegian grain elevators and compound feed mills RESEARCH ARTICLE.

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1 World Mycotoxin Journal, 25; 8 (3): Wageningen Academic P u b l i s h e r s - Friday, May 22, 25 2::5 AM - Norwegian Veterinary Institute - Section for Chemistry and Toxicology IP Address: Mycotoxins and other fungal metabolites in grain dust from Norwegian grain elevators and compound feed mills A. Straumfors *, S. Uhlig,2, G.S. Eriksen 2, K.K. Heldal, W. Eduard, R. Krska 3 and M. Sulyok 3 Department of Chemical and Biological Work Environment, National Institute of Occupational Health, P.O. Box 849 Dep., 33 Oslo, Norway; 2 Section for Chemistry and Toxicology, Norwegian Veterinary Institute, Ullevålsveien 68, 454 Oslo, Norway; 3 Centre for Analytical Chemistry, Department IFA, Tulln, University of Natural Resources and Life Sciences (BOKU), Konrad-Lorenz-Str. 2, 343 Tulln, Austria; anne.straumfors@stami.no Abstract. Introduction Employees at grain elevators and compound feed mills are exposed to large amounts of grain dust during work, frequently leading to airway symptoms and asthma (Broder et al., 984). Grain dust is a heterogeneous mixture of inorganic soil particles, plant fragments, insects and mite body parts, viable and nonviable microorganisms, and their bioactive components such as endotoxins, β- 3-glucans and mycotoxins (Halstensen et al., 27, 23) that all may exert health effects (Smith, 989). The exposure to viable and non-viable microorganisms and endotoxin has been extensively studied, and both experimental and epidemiological evidence of health effects have been Received: 2 July 24 / Accepted: 26 October Wageningen Academic Publishers RESEARCH ARTICLE Employees at grain elevators and compound feed mills are exposed to large amounts of grain dust during work, frequently leading to airway symptoms and asthma. Although the exposure to grain dust, microorganisms, β- 3-glucans and endotoxins has been extensively studied, the focus on the mycotoxin content of grain dust has previously been limited to one or few mycotoxins. Our objective was therefore to screen settled grain dust from grain elevators and compound feed mills for fungal metabolites by LC/MS-MS and explore differences between work places, seasons and climatic zones. Seventy fungal metabolites and two bacterial metabolites were detected. Trichothecenes, depsipeptides, ergot alkaloids, and other metabolites from Fusarium, Claviceps, Alternaria, Penicillium, Aspergillus, and other fungi were represented. The prevalence of individual metabolites was highly variable, and the concentration of each metabolite varied considerably between samples. The prevalence and concentration of most metabolites were higher in grain elevators compared to compound feed mills. Differences between seasons and climatic zones were inconclusive. All samples contained multiple mycotoxins, indicating a highly complex pattern of possible inhalational exposure. A mean exposure of 2 ng/m 3 of fungal metabolites was estimated, whereas a worst case scenario estimated as much as µg/m 3. Although many of these compounds may be linked to toxicological and immunological effects through experimental or epidemiological studies, it still remains to be determined whether the detected concentrations implicate adverse health outcomes when inhaled. Keywords: inhalation, occupational health, occupational exposure, mycotoxin mixture, settled dust, co-occurrence reported (Health Council of the Netherlands, 2). However, the significance of fungal metabolites in dust particles on human health is currently unclear. Mycotoxins are fungal metabolites that may exert immunosuppressive, endocrine, carcinogenic and toxic effects on humans and animals (CAST, 23). The health risks from ingesting mycotoxin-contaminated agricultural products are widely acknowledged and to a certain extent controlled, but it is unclear whether the inhalation of mycotoxin containing dust during crop handling represents an occupational health risk. Trichothecenes are a diverse group of sesquiterpene mycotoxins that are highly toxic (Creasia et al., 99; Pang et al., 988; ISSN print, ISSN online, DOI.392/WMJ

2 A. Straumfors et al. Thirty-three samples of settled grain dust (.5-5 g) were collected from 2 Norwegian grain elevators and compound feed mills in 9 municipalities in 9 counties during winter 28 (n=9), autumn 28 (n=5) and winter 29 (n=9). In the grain elevators, various grain was loaded into the elevator, sorted, winnowed, dried, rotated, moved, stored and unloaded on a continuously basis. Grain moving was either air-driven (suck-and-blow), elevator-driven, or done by passive emptying by gravity. In the compound feed mills, the grain was milled and mixed with other nutrients such as maize, calcium carbonate, fat, vitamins, and amino acids, pressed into feed pellets and filled into sacks or tanks. In autumn a large part of the grain loaded into the grain elevator came from local producers and could include humid batches that needed drying. In winter season the delivered grain had been dried at the farms before delivery, and the amount of imported grain was higher than in autumn. The activity was highest in autumn. Samples of grain dust that had newly settled on the surroundings were gently collected with a spoon and/or by brushing the dust into petri dishes and transferred to tubes after arrival at the lab. Twenty-two of the samples were from grain elevator departments whereas 8 of the samples were from compound feed mill departments. Two of the samples were not possible to categorise in one of the two departments, and one sample was taken nearby the feeding system of a wood chip heating plant of the company. These samples were excluded from comparisons between departments, but were included in all other data analyses. The sampling sites span over three geographically and climatically different districts; central coastal Norway (Nord-Trøndelag, Sør-Trøndelag), southhttp:// - Friday, May 22, 25 2::5 AM - Norwegian Veterinary Institute - Section for Chemistry and Toxicology IP Address: Ren et al., 27; Schiefer and Hancock, 984), and their inhalation may result in higher toxicity than after dermal or oral exposure (Amuzie et al., 28; Creasia et al., 99; Schiefer and Hancock, 984), presumably because of higher bioavailability (Amuzie et al., 28; Petzinger and Ziegler, 2). Epidemiological studies have, furthermore, implicated that adverse health effects including cancer and reproductive outcomes are caused by inhalation of mycotoxins (Autrup et al., 99; Kristensen et al., 2; Mclaughlin et al., 987; Nordby et al., 26). The major mycotoxin classes of concern are trichothecenes, aflatoxins, fumonisins, zearalenone (ZEA) and ochratoxin A (OTA), which are produced by three genera of fungi, namely Fusarium, Aspergillus and Penicillium (CAST, 23). Fusarium-related trichothecenes have drawn a lot of attention due to their toxicity and to the fact that their producers are plant pathogens, causing plant diseases reducing grain quality and leading to crop losses in grain cultivation. The most commonly occurring trichothecenes in grain worldwide are deoxynivalenol (DON) and its acetylated derivatives, nivalenol (NIV), T-2 toxin (T-2) and HT-2 toxin (HT-2). The mycotoxins that may occur in grain dust are identical to those that are commonly found in grain, although in higher concentrations (Halstensen et al., 26a; Krysinska-Traczyk et al., 27; Sanders et al., 23, 24). The mycotoxin content of the grain dust will indirectly reflect which fungi that have been active at one or several stages in the grain production chain. Fungal growth and production of mycotoxins are firstly depending on climatic conditions, secondly on crop type and its fungal resistance, and thirdly on the handling and storage conditions of harvested crops. Handling of grain from different sources, grain elevator and compound feed mills technology and operator routines will additionally influence the generation of dust and subsequently the exposure risk of the workers. At least twenty different mycotoxins have been detected in settled and airborne grain dust (Halstensen et al., 28). Previous studies are mostly limited to one or few mycotoxins, whereas crops and dust often are contaminated with many mycotoxins and other fungal metabolites produced either from the same or from different fungal species. As the combined exposure to multiple mycotoxins may have additive, interaction or synergistic effects (Grenier and Oswald, 2), the co-occurrence of mycotoxins is of great interest in the assessment of health risks from exposure to grain dust. The exposure to combined mycotoxins has in some cases been shown to exert greater toxicity and carcinogenicity than exposure to single mycotoxins (Bouaziz et al., 23; Kouadio et al., 27). State-of-the-art LC-MS instrumentation allows simultaneous analysis of a large number of different compounds, e.g. fungal metabolites (Abia et al., 23; Sulyok et al., 26, 2; Vishwanath et al., 29). In order to obtain an overview over the real contamination of a variety of samples, a targeted multiplex LC-MS assay has been developed over the last decade that allows for simultaneous quantification or semi-quantification of more than 3 different metabolites primarily of fungal origin (Shephard et al., 23; Uhlig et al., 23; Vishwanath et al., 29). When studying the exposure and health risks of grain handlers it is important to consider the composition of the mycotoxin mixture in the dust and any possible differences between work places. Knowledge of commonly co-occurring metabolites in grain dust can further provide the basis for future toxicological and epidemiological studies on combined effects. The objective of this study was therefore to determine the co-occurrence of more than 3 fungal metabolites in grain dust from Norwegian grain elevators and compound feed mills and explore differences between work places, seasons and climatic zones. 2. Materials and methods Sampling and sampling sites 362 World Mycotoxin Journal 8 (3)

3 Fungal metabolites in the grain industrial work environment - Friday, May 22, 25 2::5 AM - Norwegian Veterinary Institute - Section for Chemistry and Toxicology IP Address: eastern Norway (Oslo, Østfold, Vestfold, Telemark) and eastern inland of Norway (Buskerud, Hedmark, Oppland). All districts are located north of 59 degrees northern latitude. The samples were stored at -2 C until analysis. Semi-quantitative multi-mycotoxin analysis using LC-MS/MS Dust samples were weighed and transferred to 5-ml centrifuge tubes (Greiner Bio-One GmbH, Frickenhausen, Germany). The analytical method consisted of three steps: extraction using a mixture of acetonitrile:water:acetic acid (79:2:, v/v/v), dilution using a mixture of acetonitrile:water:acetic acid (2:79:, v/v/v) and direct analysis using a QTRAP 55 LC-MS/MS System (AB SCIEX, Foster City, CA, USA) equipped with a Turbo Ion Spray electrospray ionisation (ESI) source and a 29 Series HPLC System (Agilent Technologies, Inc., Santa Clara, CA, USA). The weight of individual dust samples varied between.5 and 5. g. The matrix-to-solvent ratio was :4, i.e. a.5 g dust sample was extracted with 2 ml and a 5 g dust sample was extracted with 2 ml of extraction solvent. Details on the analysis method can be inferred from the literature (Sulyok et al., 2; Taubel et al., 2; Vishwanath et al., 29). The validation and thus the determination of the limits of detection/quantification (LOD/LOQ) for grain dust samples were far beyond the scope of our study. However, the method s LOD for mycotoxins in maize has been determined to be in the lower µg/kg or ng/kgrange (Malachova et al., 24). For example, the LOD for aflatoxin B in maize has been determined to.6 µg/kg, that of ochratoxin A to.7 µg/kg and that of DON to 5.4 µg/kg. It is reasonable to anticipate that the LOD s for individual fungal metabolites in grain dust are comparable. Data analysis Non-parametric statistics were applied to the data set due to the skewed distribution of metabolite concentrations. Percentages of positive samples (=prevalence), median of the positive samples and maximum values were calculated for each metabolite. Prevalence differences between groups were tested with Pearson s Chi-square test. Subsequently, the positive samples were selected and differences in the metabolite concentration between groups were tested by the Mann-Whitney U test (two groups) or Kruskal Wallis t-test (more than two groups). Differences with P-level.5 were regarded significant. Exposure estimates were computed for metabolites with prevalence >8%. The concentrations in samples that did not contain quantifiable concentrations of these metabolites were estimated as the lowest observed value divided by the square root of 2 in order to include all samples in the data analyses. The grain workers mean and worst case inhalational exposure was estimated by multiplying the arithmetic mean and maximum concentration of individual metabolites in the settled dust with the arithmetic mean and maximum concentration of airborne grain dust. The workers exposure to airborne grain dust was measured at the same time point as the collection of settled grain dust, and is reported elsewhere (Halstensen et al., 23). 3. Results Occurrence of fungal metabolites in settled grain dust Seventy fungal metabolites and two bacterial metabolites were detected in the samples (Table ). Trichothecenes, depsipeptides, ergot alkaloids, and other metabolites from Fusarium, Claviceps, Alternaria, Penicillium, Aspergillus, and other fungi were represented. The prevalence of individual metabolites was highly variable, and the concentration of each metabolite varied considerably between samples. Most samples contained both type A and B-trichothecenes, and the concentrations of the type-b trichothecene DON was in the mg/kg range. Fungal depsipeptides were detected in all samples, with particularly high concentrations of Enniatin A (ENN A ) and B (ENN B ). The Fusarium metabolites ZEA, aurofusarin, avenacein Y, moniliformin (MON), culmorin and equisetin, the Alternaria metabolite alternariol methyl ether and the Penicillium metabolite mycophenolic acid were also present in all samples. Furthermore, a high proportion of the samples contained fumonisins, which is especially important to note as these fungal polyketides are usually absent in Norwegian grain due to the lack of the producing Fusarium species. Also other fungal metabolites, such as apicidin, emodin, monocerin, tryptophol and skyrin were present in nearly all or all samples. The largest quantities of detected metabolites in the grain dust were related to the genus Fusarium. Grain elevator versus compound feed mills The type A-trichothecene neosolaniol (NEO), several ergot alkaloids, OTA, viomellin and meleagrin were detected in samples from grain elevators only (Table ). The prevalence of the ergot alkaloid chanoclavine, the Fusarium metabolite FUM B3, the Penicillium and Aspergillus metabolites asterric acid, cyclopenol, cyclopenine, 3-methoxy-viricadin, the fungal metabolites calphostin C and skyrin, as well as the bacterial metabolites nonactin and monactin was higher in grain elevators than in compound feed mills. All samples in both grain elevators and compound feed mills contained Fusarium-related ENNs and beauvericin (Table ), but the concentrations of ENNs were significantly higher in the grain elevators compared to the compound feed mills (P<. to P=.6; table ). Similarly, the concentration of avenacein Y, apicidin, curvularin and emodin was highest in grain elevators (P=.3 to.2), whereas the concentration of dechlorogriseofulvin and brevianamid F were higher in compound feed mills (P=.5 and P<., respectively). World Mycotoxin Journal 8 (3) 363

4 A. Straumfors et al. - Friday, May 22, 25 2::5 AM - Norwegian Veterinary Institute - Section for Chemistry and Toxicology IP Address: Table. Fungal and bacterial metabolites in dust from grain elevators and compound feed mills. Metabolite All samples (n=33) Grain elevators (n=22) Compound feed mills (n=8) Significance 2 Positive (%) Median Max Positive (%) Median Max Positive (%) Median Max MW χ 2 Type-A trichothecenes T-2 tetraol T-2 toxin HT-2 toxin 97 47, , NEO Type-B trichothecenes Nivalenol Deoxynivalenol,57,279,33, ,67 Deoxynivalenol-3- glucoside acetyl-deoxynivalenol Depsipeptides Enniatin A 6, *** Enniatin A 46 7, , ** Enniatin B 783 2, , *** Enniatin B 934 9,98,37 4, *** Enniatin B *** Enniatin B ** Beauvericin Zearalenone and related compounds Zearalenone β-zearalenol Zearalenone-4-sulphate Ergot alkaloids Chanoclavine ** Agroclavine Fumigaclavine Ergometrine Ergometrinine * Ergocristine Ergocristinine * Ergosine Various Fusarium metabolites Chlamydosporols Aurofusarin 5,55 44,76 7,597 44,76 3,3 9,454 Avenacein Y 3,49,596 4,826, ,69 ** Monoliformin 5 2,7 8 2, Butenolide , , Culmorin,72,45,76, ,72 5-OH-culmorin , , Equisetin Fumonisin B , , Fumonisin B Fumonisin B * Various Alternaria metabolites Alternariol Alternariol-OMe Altertoxin-I Tentoxin World Mycotoxin Journal 8 (3)

5 Fungal metabolites in the grain industrial work environment - Friday, May 22, 25 2::5 AM - Norwegian Veterinary Institute - Section for Chemistry and Toxicology IP Address: Table. Continued. Metabolite All samples (n=33) Grain elevators (n=22) Compound feed mills (n=8) Significance 2 Positive (%) Season and climatic zones Median Max Positive (%) The prevalence of ergometrin and asterric acid was significantly higher in dust collected in the winter season compared with the autumn season (χ 2 ; P=.4 and P=.5, respectively), whereas the prevalence of cyclopeptine was higher in autumn season (P=.4). NEO was not detected in autumn samples. Significant seasonal differences in fungal metabolite concentrations could not be observed among Median Max Positive (%) Median Max MW χ 2 Penicillium and Aspergillus metabolites Sterigmatocystin Mycophenolic acid Ochratoxin A * Dechlorogriseofulvin ** Averufin Asterric acid ** Cyclopenol , , * Cyclopenine * Viridicatin * 3-OMe-viridicatin *** Viomellin 39 67, ,726 * Terphenyllin Cyclopeptine Brevianamid F *** Meleagrin Other fungal metabolites 3-nitropropionic acid Monocerin Tryptophol Rubellin D Apicidin * Secalonic acid D Curvularin A ** Cyclosporin C 36 76, , Calphostin C * Methylsulochrin Emodin ** Chrysophanol Skyrin * Physcion A , , Bacterial metabolites Nonactin * Monactin * Median of positive samples. 2 Level of significance of Mann-Whitney U test (MW) or Person Chi square (χ 2 ) between grain elevators and compound feed mills;* P.5; ** P.; *** P.. the positive samples. However, the concentration of the bacterial metabolite nonactin was significantly higher in autumn (median.8 µg/kg, max. 6.7 µg/kg) compared with winter season (median.8 µg/kg, max. 3.5 µg/kg) (P=.2). The distribution across the three different climatic zones was significantly different for twenty of the metabolites (result not shown). However, neither the distribution of depsipeptides nor Aspergillus and Penicillium metabolites differed between climatic zones. World Mycotoxin Journal 8 (3) 365

6 A. Straumfors et al. - Friday, May 22, 25 2::5 AM - Norwegian Veterinary Institute - Section for Chemistry and Toxicology IP Address: Co-occurrence of fungal metabolites There was high degree of co-occurrence of different metabolites in all samples (Figure ). Some of the metabolites were strongly correlated within their group. Strong correlations were observed between the detected type A trichothecenes (r= , P=. to P>.), except NEO, which was present in only 3% of the samples and did not correlate with any of the other type A trichotehecenes. NEO was not present in compound feed mills. All type B trichothecenes were strongly correlated (r= ; P=.6 to P<.). μg/kg μg/kg, A C, Sample number Sterigmatocystin Mycophenolic acid Ochratoxin A Dechlorogrise ofulvin Asterric acid Cyclopenol/ -penine Viridicadin/ -3-OMe Viomellein Terphenyllin Cyclopeptine Brevianamid F Meleagrin The spearman correlation between DON and DON-3- glucoside was.78, P<. (Figure 2A). Strong correlations were observed between all depsipeptides (r= , P<.), except beauvericin, which did not correlate with any of the ENNs, although all depsipetides were present in all samples. The correlation between ZEA and ZEA-4- sulphate was.94, P<. (Figure 2B). Culmorin correlated strongly with its 5-OH-derivative (r s =.68, as well as the unrelated aurofusarin (r s =.82), (Figure 2C). All Alternaria metabolites were strongly mutually correlated (r=.5-.86, P=. to P<.). Particularly strong was the correlation between alternariol-methylether and alternariol, as well as altertoxin- and alternariol (Figure 2D). B,, Sample number , Type A- trichothecenes Type B- trichothecenes ZEA/ZEA- 4-sulphate ENNs Beauvericin Ergot alkaloids Alternariol/ Alternariol-OMe Altertoxin I Tentoxin D Chlamydosporols Aurofusarin Avenacein Y Moniliformin Butenolide Culmorin/ 5-OH-culmorin Equisetin Fumonisins alpha-3- nitropropionic acid Monocerin Tryptophol Rubellin D Apicidin Secalonic acid D Curvularin A Cyclosporin C Calphostin C Methylsulochrin Emodin Chrysophanol Skyrin Physcion A Figure. Co-occurrence plots of mycotoxins and fungal metabolites in dust from grain elevators and compound feed mills. Samples -8 were collected in compound feed mills, samples 9-3 were collected in grain elevators. Samples 3-32 were not categorised, and sample 33 was collected nearby the feeding system of the wood chip heating plant of one of the companies. Co-occurrence of mycotoxins and fungal metabolites in each sample was plotted according to importance and toxicity; major Fusarium mycotoxins, ergot alkaloids, depsipeptides and Alternaria metabolites (A), various other Fusarium metabolites (B), various Penicillium and Aspergillus metabolites (C) and various other fungal metabolites (D). Several closely related metabolites were combined to improve readability: In plot A, all type A trichotehcenes, all type B trichothecenes, zearalenone (ZEA) and ZEA-4-sulphate, enniatins, ergot alkaloids, alternariol and alternariol-methyl-ether, respectively, were grouped together to make the plots clearer. In plot B, culmorin and 5-hydroxy-culmorin, and all fumonisins, respectively, were grouped together. In plot C, cyclopenol and cyclopenine, viridicadin and viridicadin-3-methyl-ether, respectively, were grouped together. 366 World Mycotoxin Journal 8 (3)

7 Fungal metabolites in the grain industrial work environment - Friday, May 22, 25 2::5 AM - Norwegian Veterinary Institute - Section for Chemistry and Toxicology IP Address: DON-3-glucoside (μg/kg) μg/kg , A C 5-OH-Culmorin Aurofusarin 5-OH-Culmorin: r s =.68 P<. n=27 Potential inhalational exposure, Deoxynivalenol Culmorin (μg/kg), r s =.78 P<. n=33 Aurofusarin: r s =.82 P<. n=33, The highest potential inhalational exposure came from various Fusarium metabolites, which were present in highest concentrations in the dust (Figure 3). The estimated mean exposure to Fusarium metabolites, including trichothecenes and aurofusarin (not included in Figure 3), was below 2 ng/m 3, whereas the worst case exposure was nearly µg/m 3., Zearalenone (μg/kg) μg/kg B D Alternariol-OMe Altertoxin-I Alternariol-OMe: r s =.63 P<. n=33 4. Discussion Zearalenone-4-sulphate Alternariol (μg/kg) r s =.94 P<. n=29 Altertoxin-I: r s =.86 P<. n=27 Figure 2. Scatter plots of selected metabolite correlations. (A) Deoxynivalenol (DON) versus DON-3-glycoside; (B) Zearalenone (ZEA) versus ZEA-4-sulphate; (C) culmorin versus 5-hydroxy-culmorin and aurofusarin, respectively; (D) alternariol versus alternariol-methyl ether and altertoxin, respectively. The spearman correlation coefficient r s, P-value and number or samples is given for each correlation plot. The present study is to our knowledge the broadest characterisation of mycotoxin occurrence in settled grain dust from grain elevators and compound feed mills. Several fungal metabolites that had previously never been detected in grain or grain dust were demonstrated, in addition to mycotoxins commonly occurring in grain, such as DON, T-2 and HT-2. Trichothecenes, fumonisins, ZEA and OTA, mycotoxin groups of major concern, were represented. While aflatoxins, representing highly carcinogenic compounds, were not detected in the samples, the related World Mycotoxin Journal 8 (3) 367

8 A. Straumfors et al. - Friday, May 22, 25 2::5 AM - Norwegian Veterinary Institute - Section for Chemistry and Toxicology IP Address: Zearalenone and related compounds Various Fusarium metabolites Various Alternaria metabolites Trichothecenes Penicillium and Aspergillus toxins Other fungal metabolites Ergot alkaloids Depsipeptides Bacterial metabolites Zearalenone and related compounds Various Fusarium metabolites Various Alternaria metabolites Trichothecenes Penicillium and Aspergillus toxins Other fungal metabolites Ergot alkaloids Depsipeptides Bacterial metabolites compound sterigmatocystin was detected in several of the samples. Sterigmatocystin is an aflatoxin precursor in some Aspergillus spp, while the compound is apparently not converted to aflatoxins in Aspergillus versicolor (Alkhayyat and Yu, 24). Mycotoxins have been found in settled grain dust from corn processing plants in Georgia, USA (aflatoxins) (Silas et al., 987), in grain elevators in New Orleans (ZEA, but no aflatoxin or OTA) (Palmgren et al., 983), from threshing on Polish farms (MON, NIV, DON and OTA) (Krysinska- Traczyk et al., 2, 27), in German grain elevators (OTA, A B 2 4 Mean exposure (ng/m 3 ) 2, Max exposure (ng/m 3 ) 6 3, DON and ZEA) (Mayer et al., 27), and from threshing and storage work on Norwegian farms (HT-2, T-2, DON, NIV, diacetoxyscirpenol and OTA) (Halstensen et al., 24; Nordby et al., 24). The median concentrations of the majority of these mycotoxins were 2-7 times higher in the present study. The detection of a number of Penicillium, Aspergillus and Fusarium toxins in farms and storage facilities in Belgium was one of the first studies that utilised a multi-mycotoxin LC/MS-MS approach (Tangni and Pussemier, 27) in an occupational setting. The development of the LC/MS-MS 8 4, Metabolite Alternariol Alternariol-OMe Altertoxin I Apicidin Avenacein Y Beauvericin Brevianamid F Butenolide Chanoclavine Culmorin Cyclopenol Deoxynivalenol DON-3-glucoside Emodin Enn A Enn A Enn B Enn B Enn B2 Enn B3 Equisetin Ergometrine HT-2 Moniliformin Monocerin Mycophenolic acid Nivalenol Nonactin OH-culmorin OMe-viridicatin Physcion Skyrin T-2 T-2-teratol Tryptophol Zearalenone ZEA-4-sulphate Figure 3. Estimated inhalable exposure to mycotoxins and fungal metabolites during work in grain elevators and compound feed mills. Mycotoxins and metabolites with prevalence above 8% were included in the estimates and stacked in group-based bars. Aurofusarin was excluded from the figure due to a very high mean and maximum concentration that precluded the contribution from all other mycotoxins in the stacked bar chart. 368 World Mycotoxin Journal 8 (3)

9 Fungal metabolites in the grain industrial work environment - Friday, May 22, 25 2::5 AM - Norwegian Veterinary Institute - Section for Chemistry and Toxicology IP Address: method for the detection of microbial metabolites used in the present study started in 26 (Sulyok et al., 26) and has previously been used to screen the metabolic profile in the waste management sector (Mayer et al., 2) and indoor air (Peitzsch et al., 22; Taubel et al., 2). Higher numbers of microbial secondary metabolites and at higher levels were found in settled dust derived from moisture damaged damp schools compared to schools not affected by moisture damage and dampness (Peitzsch et al., 22). It was suggested that the normal fungal metabolite spectrum shifted due to increased water activity following building dampness. The metabolites detected in the grain dust reflect the commonly observed infection of Norwegian grain with certain fungal species. As expected, a majority of the detected metabolites were from Fusarium typically found in grain in Norway. Fusarium langsethiae is the main producer of type A trichothecenes in Norway, whereas type B trichothecenes and ZEA are produced by Fusarium graminearum and Fusarium culmorum. Fusarium avenaceum is likely responsible for the observed contamination with MON, ENNs and avenacein Y (Uhlig et al., 27). The detection of ENNs in all samples demonstrate the widespread contamination of grain with the latter species, and the concentration of ENN A and B was considerably higher than previously found in samples from waste recycling plants (Mayer et al., 2). The contamination with DON, DON-3-glucoside and 3-acetyl-DON is most likely related to F. graminearum and F. culmorum (Langseth et al., 2). Culmorin is also produced by these species, and the cooccurrence with DON in all samples was therefore expected and in accordance with previous reports showing that culmorin compounds often occur together with type- B-trichothecenes (Ghebremeskel and Langseth, 2). More exotic for Scandinavian samples was the detection of fumonisins, as the producers, Fusarium verticillioides and Fusarium proliferatum, are rarely observed in Norway. Fumonisins are commonly contaminating maize crops, and were in this connection most likely derived from imported maize used in the compound feed production. The higher fumonisin concentration in compound feed mills most likely reflects the use of the contaminated imported maize in the compound feed production. Periodical storage of maize in the grain elevator departments could be a reason for the presence of fumonisins also in grain elevators, and not only the compound feed departments. The occurrence of several Alternaria metabolites was high in the analysed samples (76%-%). Although the observed occurrence in our study was significantly higher than the 6% prevalence of alternariol-methylether reported in a recent EFSA opinion on Alternaria toxins in food and feed (EFSA, 2), it is in accordance with the prevalence previously reported from Norwegian grain (Uhlig et al., 23). The concentrations were, however, higher in grain dust than in grain. This was also observed for several other mycotoxins. Higher concentrations of mycotoxins in grain dust compared to the grain itself have been reported previously (Halstensen et al., 26b; Krysinska-Traczyk et al., 27; Sanders et al., 23, 24), and is probably because the grain dust is enriched with particles from the outer shell layer of the grain where the mycotoxin concentrations are higher than the whole grain. A relatively high number of samples (56%) contained sterigmatocystin, a metabolite that is structurally closely related to the aflatoxins and has similar toxic effects as aflatoxin B, but is considered to be less potent (EFSA, 23). A similar high prevalence of sterigmatocystin, but with a lower mean concentration, has been found in Norwegian oats, whereas the content in barley and wheat was significantly lower (Uhlig et al., 23). The concentration of nonactin and monactin in the present study was in the same range as previously found in settled dust from paper waste, but lower than found in municipal waste samples (Mayer et al., 2). It is difficult to explain all the observed differences in prevalence and concentration of metabolites seen between grain elevators and compound feed mills. However, the main contributors are likely to be the different raw materials being processed in the two departments. The higher concentration levels of many grain-related mycotoxins in grain elevators compared with compound feed mills was expected since the dust in compound feed mills are not only generated from grain, but also from other raw materials. On the other hand, the other raw materials may contain other metabolites not present in the grains. The ergot alkaloids, produced by Claviceps purpurea that parasitises the ears of grain, especially rye, the type A trichothecene NEO, produced by F. langsethiae and Fusarium sporotrichioides, and OTA, produced by the so-called storage fungi Aspergillus ochraceus and Penicillium verrucosum, was found in grain elevators only. Dechlorogriseofulvin was found in significantly higher concentration in the compound feed mills compared to the grain elevators. This metabolite is produced by Penicillium griseofulvum and other Penicillium species and have mycostatic activity against a variety of fungi, but is also commercially produced. Dechlorogriseofulvin has previously been found in one settled dust sample of municipal waste (Mayer et al., 2). The observed differences between seasons and climatically different zones for certain metabolites were difficult to explain, and could be due to coincidence. The growth of fungi and their production of mycotoxins are generally dependent on weather, humidity, temperature, climate or geographic locations, as well as agricultural factors such as fungicide usage, ploughing routines and plant resistance. The mycotoxin prevalence may vary from year to year according to these determinants. The samples in the present study are collected in three seasons and three climatic zones and should thus include a fairly representative variation in this regard. The dominant fungal species and World Mycotoxin Journal 8 (3) 369

10 A. Straumfors et al. - Friday, May 22, 25 2::5 AM - Norwegian Veterinary Institute - Section for Chemistry and Toxicology IP Address: the mycotoxins they produce may vary from one part of the world to another, depending on differences in topography and climate, but also on the local level (Amend et al., 2; Krysinska-Traczyk et al., 2, 27; Mayer et al., 27; Nordby et al., 24; Peitzsch et al., 22). As Norwegian grain elevators and compound feed mills commonly also use imported grain, this adds to the complexity of seasonal and climatic variability that determines mycotoxin presence. Correlations within groups of metabolites are likely due to more or less simultaneous production of these metabolites by the same producer (e.g. DON and acetylated derivatives). DON is partly converted to the less toxic DON-3-glucoside both by the producer and in planta, but the possibility of this masked mycotoxin DON-3-glucoside to be unmasked in vivo makes it important to include in the mycotoxin analyses and risk assessments (Nagl et al., 24). Likewise, ZEA-4-sulphate may be converted back to the oestrogenbinding ZEA in vivo, and exert hormonal effects (Plasencia and Mirocha, 99). Our observation of a strong correlation between DON and DON-3-glucoside and between ZEA and ZEA-4-sulphate may in this regard be useful. As many Fusarium species produce aurofusarin, the very high concentration of this pigment in all samples could be expected, and this was probably the reason for the strong correlation with many of the other metabolites (data not shown). The correlation was particularly strong with other metabolites with high concentrations, such as culmorin. Although the relationship between ingestion of mycotoxin and human health effects has been clearly established, health effects from inhalation are still under debate. However, toxicological studies indicate strong toxic effects of trichothecenes after inhalation (Creasia et al., 99; Pang et al., 988; Schiefer and Hancock, 984). Furthermore, the basic mode of action of many of the detected metabolites is known, and may therefore indicate potential effects after inhalation. Mycophenolic acid is an immunosuppressant that was present in all samples, but in low levels. Sterigmatocystin is genotoxic in vitro similar to aflatoxin, although less hepatogenic (Jaksic et al., 22). Sterigmatocystin has been reported only once in Norway previously (Uhlig et al., 23). Two of the detected Alternaria metabolites, altertoxin- and alternariol OMe are known to have genotoxic potential. The possible inhalational effect of the high concentration of ENNs observed in all grain dust samples is uncertain since their significance in vivo is unknown. However, the compounds have recently been demonstrated to interfere with lysosomes (Ivanova et al., 22) and immunological responses (Gammelsrud et al., 22) in vitro. Thus, a potential effect of ENNs alone or in combination with other mycotoxins affecting the same parameters cannot be excluded. Exposure to multiple mycotoxins can lead to extremely complicated biological responses within a relatively simple system like a single cell. Understanding the mode of action of individual mycotoxins in simple in vitro systems can provide a rational basis for studying or predicting effects of mycotoxin mixtures (Speijers and Speijers, 24; Wan et al., 23). Different toxicological parameters and experimental procedures have been used in animal studies (Huff et al., 986; Smith et al., 997; Theumer et al., 23; Wangikar et al., 24) and in vitro tests (Bensassi et al., 24; Bernhoft et al., 24; Braunberg et al., 994; Ndossi et al., 22; Solhaug et al., 23; Tammer et al., 27; Wan et al., 23) of combined effects of multiple mycotoxin exposure. Several prediction tools have been investigated (Heussner et al., 26; Li et al., 24; Tajima et al., 22). In general, most of the mycotoxin mixture studies have observed additive and/or synergistic interactions, depending on the mixture and chosen endpoint. The effect of a mycotoxin mixture cannot therefore be predicted from the effect of the individual mycotoxins (Tajima et al., 22). Mycotoxins can also act synergistically with other bioactive microbial components such as allergens, endotoxins and microbial volatile organic components, to amplify cellular responses in vitro and in vivo (Islam and Pestka, 26; Kankkunen et al., 29; Zhou et al., 2). As grain dust also consists of several bioactive components, grain handlers may be affected by such interactions. Settled dust from grain elevators has been shown to exert moderate to high cytotoxicity in the MTT (3-(4,5-dimethylthiazol-2-yl)-2,5- diphenyltetrazolium bromide) assay (Mayer et al., 27). However, the cytotoxicity was not correlated with OTA or DON concentrations, indicating the presence of other cytotoxic agents in the grain dust. The estimated personal mean exposure of all detected fungal metabolites in the present study was below 2 ng/m 3. This may seem low, but the effect level of each metabolite is not known and neither is the combined effect of all metabolites. In a worst case scenario, the workers may inhale up to µg/m 3 of fungal metabolites during a work shift. The actual inhaled dose will depend on the work intensity. To exemplify, an adult will breathe around 3 l/min during moderate physical activity. During an 8 h shift with moderate activity, a worker will thus inhale 4 m 3 of air, and the worst case daily inhaled metabolite dose will be 44 µg. Presently, we cannot decide whether adverse levels can be reached under different scenarios of inhalational exposure, as no studies of human effects of airborne mycotoxins are known. Furthermore, the exposure data in the present study should be used with caution since they are estimations, and not direct exposure measurements. However, as no studies of airborne multiple mycotoxin exposure so far exists, this may be a useful proxy. The grain dust samples in the present study also contained a range of fungal metabolites for which very little toxicological information is available. The potential effects on human health both from oral and inhalational 37 World Mycotoxin Journal 8 (3)

11 Fungal metabolites in the grain industrial work environment - Friday, May 22, 25 2::5 AM - Norwegian Veterinary Institute - Section for Chemistry and Toxicology IP Address: exposure to these potentially bioactive compounds should therefore be subject for further study. At present it is not feasible to assess the precise effects of the multiple exposures that grain dust represents. However, an important first step is to characterise the contents of the dust to be able to evaluate the existence of potential combination effects. Characterisation of the exposure patterns of fungal metabolites in different occupations will not only create knowledge of indicative concentrations of prevalent compounds, but also give a basis for evaluating the exposure differences qualitatively. This may further be used in a more focused risk assessment in the various occupational surroundings. 5. Conclusions Over 7 microbial metabolites were detected in settled dust from grain elevators and compound feed mills. The main mycotoxins found were from the genus Fusarium. Particularly large quantities of DON, depsipeptides, aurofusarin, avenacein Y and culmorin were found. Most of the metabolites have previously not been detected in grain dust, and for some very little toxicological information is available. The prevalence and concentration of most metabolites were higher in grain elevators compared to compound feed mills. All samples contained multiple mycotoxins, indicating a highly complex pattern of possible inhalational exposure. Although many of these compounds may be linked to toxicological and immunological effects through experimental and epidemiological studies, it remains to be determined whether the detected concentrations of the microbial metabolites are of toxicological relevance and may implicate adverse health outcomes when inhaled. Acknowledgements Thanks are due to Per Ole Huser for participating in field work. This work was financially supported by The Confederation of Norwegian Enterprise (S-2585). The LC MS/MS system was funded by the Federal Country Lower Austria (grant number: Technopol 85) and cofinanced by the European regional development fund of the European Union. References Abia, W.A., Warth, B., Sulyok, M., Krska, R., Tchana, A.N., Njobeh, P.B., Dutton, M.F. and Moundipa, P.F., 23. Determination of multi-mycotoxin occurrence in cereals, nuts and their products in Cameroon by liquid chromatography tandem mass spectrometry (LC-MS/MS). Food Control 3: Alkhayyat, F. and Yu, J.H., 24. Upstream regulation of mycotoxin biosynthesis. Advances in Applied Microbiology 86: Amend, A.S., Seifert, K.A., Samson, R. and Bruns, T.D., 2. Indoor fungal composition is geographically patterned and more diverse in temperate zones than in the tropics. Proceedings of the National Academy of Sciences of the USA 7: Amuzie, C.J., Harkema, J.R. and Pestka, J.J., 28. Tissue distribution and proinflammatory cytokine induction by the trichothecene deoxynivalenol in the mouse: Comparison of nasal vs. oral exposure. Toxicology 248: Autrup, J.L., Schmidt, J., Seremet, T. and Autrup, H., 99. Determination of exposure to aflatoxins among Danish workers in animal-feed production through the analysis of aflatoxin-b adducts to serum-albumin. Scandinavian Journal of Work Environment & Health 7: Bensassi, F., Gallerne, C., Sharaf El Dein, O., Hajlaoui, M.R., Lemaire, C. and Bacha, H., 24. In vitro investigation of toxicological interactions between the fusariotoxins deoxynivalenol and zearalenone. Toxicon 84: -6. Bernhoft, A., Keblys, M., Morrison, E., Larsen, H.J. and Flaoyen, A., 24. Combined effects of selected Penicillium mycotoxins on in vitro proliferation of porcine lymphocytes. Mycopathologia 58: Bouaziz, C., Bouslimi, A., Kadri, R., Zaied, C., Bacha, H. and Abid- Essefi, S., 23. The in vitro effects of zearalenone and T-2 toxins on Vero cells. Experimental and Toxicologic Pathology 65: Braunberg, R.C., Barton, C.N., Gantt, O.O. and Friedman, L., 994. Interaction of citrinin and ochratoxin A. Natural Toxins 2: Broder, I., Hutcheon, M.A., Mintz, S., Davies, G., Leznoff, A., Thomas, P. and Corey, P., 984. Changes in respiratory variables of grain handlers and civic workers during their initial months of employment. British Journal of Industrial Medicine 4: Council for Agricultural Science and Technology (CAST), 23. Mycotoxins: risks in plant, animal and human systems. Task force report No. 39. Ames, IA, USA. Creasia, D.A., Thurman, J.D., Wannemacher, R.W. and Bunner, D.L., 99. Acute Inhalation toxicity of T-2 mycotoxin in the rat and guinea-pig. Fundamental and Applied Toxicology 4: European Food Safety Authority (EFSA), 2. Scientific opinion on the risks for animal and public health related to the presence of Alternaria toxins in feed and food. EFSA Journal 9: European Food Safety Authority (EFSA), 23. Scientific opinion on the risk for public and animal health related to the presence of sterigmatocystin in food and feed. EFSA Journal : Gammelsrud, A., Solhaug, A., Dendele, B., Sandberg, W.J., Ivanova, L., Bolling, A.K., Lagadic-Gossmann, D., Refsnes, M., Becher, R., Eriksen, G. and Holme, J.A., 22. Enniatin B-induced cell death and inflammatory responses in RAW murine macrophages. Toxicology and Applied Pharmacology 26: Ghebremeskel, M. and Langseth, W., 2. The occurrence of culmorin and hydroxy-culmorins in cereals. Mycopathologia 52: 3-8. Grenier, B. and Oswald, I.P., 2. Mycotoxin co-contamination of food and feed: meta-analysis of publications describing toxicological interactions. 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12 A. Straumfors et al. - Friday, May 22, 25 2::5 AM - Norwegian Veterinary Institute - Section for Chemistry and Toxicology IP Address: Halstensen, A.S., Nordby, K.C., Eduard, W. and Klemsdal, S.S., 26a. Real-time PCR detection of toxigenic Fusarium in airborne and settled grain dust and associations with trichothecene mycotoxins. Journal of Environmental Monitoring 8: Halstensen, A.S., Nordby, K.C., Elen, O. and Eduard, W., 24. Ochratoxin A in grain dust Estimated exposure and relations to agricultural practices in grain production. Annals of Agricultural and Environmental Medicine : Halstensen, A.S., Nordby, K.C., Klemsdal, S.S., Elen, O., Clasen, P.E. and Eduard, W., 26b. Toxigenic Fusarium spp. as determinants of trichothecene mycotoxins in settled grain dust. Journal of Occupational and Environmental Hygiene 3: Halstensen, A.S., Nordby, K.C., Kristensen, P. and Eduard, W., 28. Mycotoxins in grain dust. Stewart Postharvest Review 6: -9. Halstensen, A.S., Nordby, K.C., Wouters, I.M. and Eduard, W., 27. Determinants of microbial exposure in grain farming. Annals of Occupational Hygiene 5: Health Council of the Netherlands, 2. Grain dust. Health-based recommended occupational exposure limit. Report 2/3, Health council of the Netherlands, The Hague, the Netherlands. Available at: Heussner, A.H., Dietrich, D.R. and O Brien, E., 26. In vitro investigation of individual and combined cytotoxic effects of ochratoxin A and other selected mycotoxins on renal cells. Toxicology in vitro 2: Huff, W.E., Kubena, L.F., Harvey, R.B., Hagler Jr., W.M., Swanson, S.P., Phillips, T.D. and Creger, C.R., 986. Individual and combined effects of aflatoxin and deoxynivalenol (DON, vomitoxin) in broiler chickens. Poultry Science 65: Islam, Z. and Pestka, J.J., 26. LPS priming potentiates and prolongs proinflammatory cytokine response to the trichothecene deoxynivalenol in the mouse. Toxicology and Applied Pharmacology 2: Ivanova, L., Egge-Jacobsen, W.M., Solhaug, A., Thoen, E. and Faeste, C.K., 22. Lysosomes as a possible target of enniatin B-induced toxicity in Caco-2 Cells. Chemical Research in Toxicology 25: Jaksic, D., Puel, O., Canlet, C., Kopjar, N., Kosalec, I. and Klaric, M.S., 22. Cytotoxicity and genotoxicity of versicolorins and 5-methoxysterigmatocystin in A549 cells. Archives of Toxicology 86: Kankkunen, P., Rintahaka, J., Aalto, A., Leino, M., Majuri, M.L., Alenius, H., Wolff, H. and Matikainen, S., 29. Trichothecene mycotoxins activate inflammatory response in human macrophages. Journal of Immunology 82: Kouadio, J.H., Dano, S.D., Moukha, S., Mobio, T.A. and Creppy, E.E., 27. Effects of combinations of Fusarium mycotoxins on the inhibition of macromolecular synthesis, malondialdehyde levels, DNA methylation and fragmentation, and viability in Caco-2 cells. Toxicon 49: Kristensen, P., Andersen, A. and Irgens, L.N., 2. Hormonedependent cancer and adverse reproductive outcomes in farmers families effects of climatic conditions favoring fungal growth in grain. Scandinavian Journal of Work Environment and Health 26: Krysinska-Traczyk, E., Kiecana, I., Perkowski, J. and Dutkiewicz, J., 2. Levels of fungi and mycotoxins in samples of grain and grain dust collected on farms in Eastern Poland. Annals of Agricultural and Environmental Medicine 8: Krysinska-Traczyk, E., Perkowski, J. and Dutkiewicz, J., 27. Levels of fungi and mycotoxins in the samples of grain and grain dust collected from five various cereal crops in eastern Poland. Annals of Agricultural and Environmental Medicine 4: Langseth, W., Ghebremeskel, M., Kosiak, B., Kolsaker, P. and Miller, D., 2. Production of culmorin compounds and other secondary metabolites by Fusarium culmorum and F. graminearum strains isolated from Norwegian cereals. Mycopathologia 52: Li, Y., Zhang, B., He, X., Cheng, W.H., Xu, W., Luo, Y., Liang, R., Luo, H. and Huang, K., 24. Analysis of individual and combined effects of ochratoxin A and zearalenone on HepG2 and KK- cells with mathematical models. Toxins 6: Malachova, A., Sulyok, M., Beltran, E., Berthiller, F. and Krska, R., 24. Optimization and validation of a quantitative liquid chromatography-tandem mass spectrometric method covering 295 bacterial and fungal metabolites including all regulated mycotoxins in four model food matrices. Journal of Chromatography A 362: Mayer, S., Curtui, V., Usleber, E. and Gareis, M., 27. Airborne mycotoxins in dust from grain elevators. Mycotoxin Res 23: 94-. Mayer, S., Vishwanath, V. and Sulyok, M., 2. Airborne workplace exposure to microbial metabolites in waste recycling plants. In: Proceedings 6 th International Scientific Conference on bioaerosols, fungi, bacteria, mycotoxins in indoor and outdoor environment and human health, Satatoga Springs. Fungal Research Group Foundation Inc. Albany, New York, NY, USA, pp Mclaughlin, J.K., Malker, H.S.R., Malker, B.K., Stone, B.J., Ericsson, J.L.E., Blot, W.J., Weiner, J.A. and Fraumeni, J.F., 987. Registrybased analysis of occupational risks for primary liver-cancer in Sweden. Cancer Research 47: Nagl, V., Wochtl, B., Schwartz-Zimmermann, H.E., Hennig-Pauka, I., Moll, W.D., Adam, G. and Berthiller, F., 24. Metabolism of the masked mycotoxin deoxynivalenol-3-glucoside in pigs. Toxicology Letters 229: Ndossi, D.G., Frizzell, C., Tremoen, N.H., Faeste, C.K., Verhaegen, S., Dahl, E., Eriksen, G.S., Sorlie, M., Connolly, L. and Ropstad, E., 22. An in vitro investigation of endocrine disrupting effects of trichothecenes deoxynivalenol (DON), T-2 and HT-2 toxins. Toxicology Letters 24: Nordby, K.C., Halstensen, A.S., Elen, O., Clasen, P.E., Langseth, W., Kristensen, P. and Eduard, W., 24. Trichothecene mycotoxins and their determinants in settled dust related to grain production. 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